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Evolutionary Consequences of Fallback Foods

  • Andrew J. Marshall
  • Richard W. Wrangham
Article

Abstract

Primatologists use the term fallback foods to denote resources of relatively low preference that are used seasonally when preferred foods are unavailable. We examine the assumption that fallback foods play an important role in shaping morphological adaptations, behavior, and socioecology in primates. We discuss operational definitions of preferred and fallback foods and suggest that the evolutionary importance of fallback foods applies more to adaptations for processing than for harvesting foods. Equally, we propose that preferred resources tend to drive adaptations for harvesting foods. We distinguish 2 classes of fallback foods according to their roles in the diet and their evolutionary effects. Staple fallback foods are available year-round, tend to be eaten throughout the year, and seasonally can constitute up to 100% of the diet. Filler fallback foods never constitute 100% of the diet, and may be completely avoided for weeks at a time. We suggest that the availability of the 2 classes of fallback foods have different effects on the socioecology of primate species.

Keywords

diet fallback foods feeding ecology resource selectivity seasonality 

Notes

Acknowledgments

Our thinking about the issues discussed here benefited substantially from numerous productive discussions with Mark Leighton, and we thank him for his input. We also thank Herman Pontzer, David Pilbeam, and 3 anonymous reviewers for helpful comments and discussion. A. J. Marshall gratefully acknowledges Conservation International and The Arnold Arboretum of Harvard University for postdoctoral support. Some of the concepts considered in this article are cogently discussed in a new book by Brockman and van Schaik (2005) that was published as this article was in its final stages of revision. Readers are encouraged to consult this volume (especially Hemingway and Bynum 2005; Knott 2005).

References

  1. Altmann, S. A. (1998). Foraging for survival. Chicago: Chicago University Press.Google Scholar
  2. Basabose, A. K. (2002). Diet composition of chimpanzees inhabiting the montane forest of Kahuzi, Democratic Republic of Congo. American Journal of Primatology, 58, 1–21.PubMedGoogle Scholar
  3. Bauchop, T. (1971). Stomach microbiology of primates. Annual Review of Microbiology, 25, 429–436.PubMedGoogle Scholar
  4. Bauchop, T. (1977). Foregut fermentation. In R. T. J. Clarke & T. Bauchop (Eds.), Microbial ecology of the gut (pp. 223–250). New York: Academic Press.Google Scholar
  5. Bauchop, T., & Martucci, R. W. (1968). Ruminant-like digestion of the langur monkey. Science, 161, 698–700.PubMedGoogle Scholar
  6. Blake, J. G., Loiselle, B. A., Moermond, T. C., Levey, D. J., & Denslow, J. S. (1990). Quantifying abundance of fruits for birds in tropical habitats. Studies in Avian Biology, 13, 73–79.Google Scholar
  7. Boag, P. T., & Grant, P. R. (1981). Intense natural selection in a population of Darwin’s finches (Geospizinae) in the Galápagos. Science, 214, 82–85.PubMedGoogle Scholar
  8. Brockman, D. K., & van Schaik, C. P. (2005). Seasonality in primates. Cambridge, U.K.: Cambridge University Press.Google Scholar
  9. Cannon, C. H., & Leighton, M. (1994). Comparative locomotor ecology of gibbons and macaques: Selection of canopy elements for crossing gaps. American Journal of Physical Anthropology, 93, 505–524.PubMedGoogle Scholar
  10. Cannon, C. H., & Leighton, M. (1996). Comparative locomotor ecology of gibbons and macaques: Does brachiation minimize travel costs? Tropical Biodiversity, 3, 261–267.Google Scholar
  11. Chapman, C. A. (1987). Flexibility in diets of three species of Costa Rican primates. Folia Primatologica, 49, 90–105.CrossRefGoogle Scholar
  12. Chapman, C. A., Wrangham, R. W., & Chapman, L. J. (1994). Indices of habitat-wide fruit abundance in tropical forests. Biotropica, 26, 160–171.Google Scholar
  13. Chesson, J. (1978). Measuring preference in selective predation. Ecology, 59, 211–215.Google Scholar
  14. Chesson, J. (1983). The estimation and analysis of preference and its relationship to foraging models. Ecology, 64, 1297–1304.Google Scholar
  15. Chivers, D. J., & Hladik, C. M. (1980). Morphology of the gastrointestinal tract in primates: Comparisons with other mammals in relation to diet. Journal of Morphology, 166, 337–386.PubMedGoogle Scholar
  16. Chivers, D. J., & Hladik, C. M. (1984). Diet and gut morphology in primates. In D. J. Chivers, B. A. Wood, & A. Bilsborough (Eds.), Food acquisition and processing in primates (pp. 213–230). New York: Plenum Press.Google Scholar
  17. Clutton-Brock, T. H., & Harvey, P. H. (1980). Primates, brains, and ecology. Journal of Zoology (London), 190, 309–323.CrossRefGoogle Scholar
  18. Cock, M. J. W. (1978). The assessment of preference. Journal of Animal Ecology, 47, 805–816.Google Scholar
  19. Conklin-Brittain, N. L., Wrangham, R. W., & Hunt, K. D. (1998). Dietary response of chimpanzees and Cercopithecines to seasonal variation in fruit abundance: II. Macronutrients. International Journal of Primatology, 19, 949–970.Google Scholar
  20. Davies, A. G. (1994). Colobine populations. In A. G. Davies, & J. F. Oates (Eds.), Colobine monkeys: Their ecology, behaviour, and evolution (pp. 285–310). Cambridge, U.K.: Cambridge University Press.Google Scholar
  21. Davies, A. G., Bennett, E. L., & Waterman, P. G. (1988). Food selection by two South-east Asian colobine monkeys (Presbytis rubicunda and Presbytis melalophos) in relation to plant chemistry. Biological Journal of the Linnean Society, 34, 33–56.Google Scholar
  22. de A. Moura, A. C., & Lee, P. C. (2004). Capuchin stone tool use in a Caatinga Dry Forest. Science, 306, 1909.Google Scholar
  23. Dittus, W. P. J. (1979). The evolution of behaviors regulating density and age-specific sex ratios in a primate population. Behaviour, 69, 265–302.Google Scholar
  24. Dominy, N. J., & Lucas, P. W. (2001). Ecological importance of trichromatic vision to primates. Nature, 410, 363–366.PubMedGoogle Scholar
  25. Dominy, N. J., Svenning, J.-C., & Li, W.-H. (2003). Historical contingency in the evolution of primate color vision. Journal of Human Evolution, 44, 25–45.PubMedGoogle Scholar
  26. Doran, D. M., McNeilage, A., Greer, D., Bocian, C., Mehlman, P., & Shah, N. (2002). Western lowland gorilla diet and resource availability: New evidence, cross-site comparisons, and reflections on indirect sampling methods. American Journal of Primatology, 58, 91–116.PubMedGoogle Scholar
  27. Dumont, E. R. (1995). Enamel thickness and dietary adaptation among extant primates and chiropterans. Journal of Mammalogy, 76, 1127–1136.Google Scholar
  28. Fleagle, J. G. (1984). Primate locomotion and diet. In D. J. Chivers, B. A. Wood & A. Bilsborough (Eds.), Food acquisition and processing in primates (pp. 105–117). New York: Plenum Press.Google Scholar
  29. Galdikas, B. M. F. (1979). Orangutan adaptation at Tanjung Puting Reserve: Mating and ecology. In D. L. Hamburg & E. R. McCown (Eds.), The great apes (pp. 195–233). London: W. A. Benjamin.Google Scholar
  30. Gaulin, S. J. C., & Konner, M. J. (1977). On the natural diets of primates, including humans. In R. J. Wurtman & J. J. Wurtman (Eds), Nutrition and the brain (pp. 1–86). New York: Raven Press.Google Scholar
  31. Goldstein, S., Post, D., & Melnick, D. (1978). An analysis of cercopithecoid odontometrics. American Journal of Physical Anthropology, 49, 517–532.PubMedGoogle Scholar
  32. Guillotin, M., Dubost, G., & Sabatier, D. (1994). Food choice and food competition among the three major primate species in French Guiana. Journal of Zoology (London), 233, 551–579.Google Scholar
  33. Hanya, G. (2004). Diet of a Japanese macaque troop in the coniferous forest of Yakusima. International Journal of Primatology, 25, 55–69.Google Scholar
  34. Hemingway, C. A., & Bynum, N. (2005). The influence of seasonality on primate diet and ranging. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in primates (pp. 57–104). Cambridge, U.K.: Cambridge University Press.Google Scholar
  35. Hylander, W. L. (1975). Incisor size and diet in anthropoids with special reference to Cercopithecidae. Science, 189, 1095–1098.PubMedGoogle Scholar
  36. Isbell, L. A. (1991). Contest and scramble competition: Patterns of female aggression and ranging behavior among primates. Behavioral Ecology, 2, 143–155.Google Scholar
  37. Isbell, L. A., Pruetz, J. D., Lewis, M., & Young, T. P. (1998). Locomotor activity differences between sympatric patas monkeys (Erythrocebus patas) and vervet monkeys (Cercopithecus aethiops): Implications for the evolution of long hindlimb length in Homo. American Journal of Physical Anthropology, 105, 199–207.PubMedGoogle Scholar
  38. Janson, C. H., & van Schaik, C. P. (1993). Ecological risk aversion in juvenile primates: slow and steady wins the race. In M. E. Pereira & L. A. Fairbanks (Eds.), Juvenile primates (pp. 57–74). Oxford: Oxford University Press.Google Scholar
  39. Janson, C. H., & Chapman, C. A. (1999). Resources and primate community structure. In J. F. Fleagle, C. Janson, & K. E. Reed (Eds.), Primate communities (pp. 237–267). Cambridge, U.K.: Cambridge University Press.Google Scholar
  40. Janson, C. H., Stiles, E. W., & White, D. W. (1986). Selection on plant fruiting traits by brown capuchin monkeys: A multivariate approach. In A. Estrada & T. H. Flemming (Eds.), Frugivores and seed dispersal (pp. 83–92). Dordrecht: Kluwer Academic.Google Scholar
  41. Johnson, D. H. (1980). The comparison of usage and availability measurements for evaluating resource preference. Ecology, 61, 65–71.Google Scholar
  42. Kawecki, T. J. (1995). Demography of source-sink populations and the evolution of ecological niches. Evolutionary Ecology, 9, 38–44.Google Scholar
  43. Kay, R. F. (1984). On the anatomical feature to infer foraging behavior in extinct primates. In P. S. Rodman & J. G. H. Cant (Eds.), Adaptations for foraging in nonhuman primates (pp. 21–53). New York: Columbia University Press.Google Scholar
  44. Kay, R. N. B., & Davies, A. G. (1994). Digestive physiology. In A. G. Davies & J. F. Oates (Eds.), Colobine monkeys: Their ecology, behaviour, and evolution (pp. 285–310). Cambridge, U.K.: Cambridge University Press.Google Scholar
  45. Kinzey, W. G. (1978). Feeding behavior and molar features in two species of titi monkey. In D. J. Chivers & J. Herbert (Eds.), Recent advances in primatology, vol. 1: Behavior (pp. 373–385). London: Academic Press.Google Scholar
  46. Knott, C. D. (1998). Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating food availability. International Journal of Primatology, 19, 1061–1079.Google Scholar
  47. Knott, C. D. (2001). Female reproductive ecology of the apes: Implications for human evolution. In P. Ellison (Ed.), Reproductive ecology and human evolution (pp. 429–463) New York: Aldine.Google Scholar
  48. Knott, C. D. (2005). Energetic responses of food availability in the great apes; implications for hominin evolution. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 351–378). Cambridge, U.K.: Cambridge University Press.Google Scholar
  49. Krebs, J. R., & Stephens, D. W. (1986). Foraging theory. Princeton, NJ: Princeton University Press.Google Scholar
  50. Laden, G., & Wrangham, R. W. (2005). The rise of the hominid as an adaptive shift in fallback foods: Plant underground storage organs (USOs) and austalopith origins. Journal of Human Evolution, 49, 482–498.PubMedGoogle Scholar
  51. Lambert, J. E. (1998). Primate digestion: Interactions among anatomy, physiology, and feeding ecology. Evolutionary Anthropology, 7, 8–20.Google Scholar
  52. Lambert, J. E. (2002). Digestive retention times in forest guenons (Cercopithecus spp.) with reference to chimpanzees (Pan troglodytes). International Journal of Primatology, 23, 1169–1185.Google Scholar
  53. Lambert, J. E., Chapman, C. A., Wrangham, R. W., & Conklin-Brittain, N. L. (2004). Hardness of cercopithecine foods: Implications for the critical function of enamel thickness in exploiting fallback foods. American Journal of Physical Anthropology, 125, 363–368.PubMedGoogle Scholar
  54. Lechowicz, M. J. (1982). The sampling characteristics of electivity indices. Oecologia, 52, 22–30.Google Scholar
  55. Lee, P. C., & Hauser, M. D. (1998). Long-term consequences of changes in territory quality on feeding and reproductive strategies of vervet monkeys. Journal of Animal Ecology, 67, 347–358.Google Scholar
  56. Leigh, S. R. (1994). Ontogenetic correlates of diet in anthropoid primates. American Journal of Physical Anthropology, 94, 499–522.PubMedGoogle Scholar
  57. Leighton, M. (1993). Modeling diet selectivity by Bornean orangutans: Evidence for integration of multiple criteria for fruit selection. International Journal of Primatology, 14, 257–313.Google Scholar
  58. Leighton, M., & Leighton, D. (1983). Vertebrate responses to fruiting seasonality within a Bornean rain forest. In S. L. Sutton, T. C. Whitmore, & A. C. Chadwick (Eds.), Tropical rain forest: Ecology and management (pp. 181–196). Boston: Blackwell.Google Scholar
  59. Lucas, P. (1979). The dental-dietary adaptations of mammals. Neues Jahrbuch für Geologies und Palaontologie, 8, 486–512.Google Scholar
  60. Lucas, P. W., & Peters, C. R. (2000). Function of postcanine tooth crown shape in mammals. In M. F. Teaford, M. M. Smith, & M. W. J. Ferguson (Eds.), Development, function, and evolution of teeth (pp. 282–289). Cambridge, U.K.: Cambridge University Press.Google Scholar
  61. Lucas, P. W., Darvell, B. W., Lee, P. K. D., Yuen, T. D. B., & Choong, M. F. (1998). Colour cues for leaf food selection by long-tailed macaques (Macaca fascicularis) with a new suggestion for the evolution of trichromatic colour vision. Folia Primatologica, 69, 139–152.Google Scholar
  62. Lucas, P. W., Dominy, N. J., Riba-Hernandez, P., Stoner, K. E., Yamashita, N., Loria-Calderon, E., et al. (2003). Evolution and function of routine trichromatic vision in primates. Evolution, 57, 2636–2643.PubMedGoogle Scholar
  63. Maas, M. C., & Dumont, E. R. (1999). Built to last: The structure, function, and evolution of primate dental enamel. Evolutionary Anthropology, 8, 133–152.Google Scholar
  64. Manly, B. J. F., McDonald, L. L., Thomas, D. L., McDonald, T. L., & Erikson, W. P. (2002). Resource selection by animals. Dordrecht: Kluwer Academic.Google Scholar
  65. Marshall, A. J. (2004). The population ecology of gibbons and leaf monkeys across a gradient of Bornean forest types. Ph.D. thesis, Department of Anthropology, Harvard University, Cambridge, MA.Google Scholar
  66. Marshall, A. J., & Leighton, M. (2006). How does food availability limit the population density of white-bearded gibbons? In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology of the apes and other primate (pp. 311–333). Cambridge, U.K.: Cambridge University Press.Google Scholar
  67. McConkey, K. R., Aldy, F., Ario, A., & Chivers, D. J. (2002). Selection of fruit by gibbons (Hylobates muelleri x agilis) in the rain forests of central Borneo. International Journal of Primatology, 23, 123–145.Google Scholar
  68. McConkey, K. R., Ario, A., Aldy, F., & Chivers, D. J. (2003). Influence of forest seasonality on gibbon food choice in the rain forests of Barito Ulu, central Kalimantan. International Journal of Primatology, 24, 19–32.Google Scholar
  69. Mills, L. S., Soule, M. E., & Doak, D. F. (1993). The keystone-species concept in ecology and conservation. Bioscience, 43, 219–224.Google Scholar
  70. Milton, K. (1981). Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. American Anthropologist, 83, 534–548.Google Scholar
  71. Milton, K. (1988). Foraging behavior and the evolution of primate cognition. In A. Whiten & R. W. Byrne (Eds.), Machiavellian intelligence: social expertise and the evolution of intellect in monkeys, apes, and humans (pp. 285–305). Oxford: Oxford University Press.Google Scholar
  72. Milton, K. (1998). Physiological ecology of howlers (Alouatta): Energetic and digestive considerations and comparison with the colobinae. International Journal of Primatology, 19, 513–548.Google Scholar
  73. Milton, K., & Demment, M. W. (1988). Digestion and passage kinetics of chimpanzees fed high and low fiber diets and comparison with human diet. Journal of Nutrition, 118, 1082–1088.PubMedGoogle Scholar
  74. Newton-Fisher, N. E. (1999). The diet of chimpanzees in the Budongo Forest Reserve, Uganda. African Journal of Ecology, 37, 344–354.Google Scholar
  75. Paine, R. T. (1969). A note on trophic complexity and community stability. American Naturalist, 103, 91–93.Google Scholar
  76. Paine, R. T. (1995). A conversation on refining the concept of keystone species. Conservation Biology, 9, 962–964.Google Scholar
  77. Peres, C. A. (2000). Identifying keystone plant resources in tropical forests: The case of gums from Parkia pods. Journal of Tropical Ecology, 16, 287–317.Google Scholar
  78. Pontzer, H. D., & Wrangham, R. W. (2004). Climbing and the daily energy cost of locomotion in wild chimpanzees: Implications for hominoid locomotor evolution. Journal of Human Evolution, 46, 317–335.PubMedGoogle Scholar
  79. Porter, L. M. (2001). Dietary differences among sympatric Callitrichinae in northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. labiatus. International Journal of Primatology, 22, 961–992.Google Scholar
  80. Potts, R. (2004). Paleoenvironmental basis of cognitive evolution in great apes. American Journal of Primatology, 62, 209–228.PubMedGoogle Scholar
  81. Power, M. E., Tilman, D., Estes, J. A., Menge, B. A., Bond, W. J., Mills, L. S., et al. (1996). Challenges in the quest for keystones. BioScience, 46, 609–620.Google Scholar
  82. Powzyk, J. A., & Mowry, C. B. (2003). Dietary and feeding differences between sympatric Propithecus diadema diadema and Indri indri. International Journal of Primatology, 24, 1143–1162.Google Scholar
  83. Regan, B. C., Juliot, C., Simmen, B., Viénot, F., Charles-Dominique, P. C., & Mollon, J. D. (2001). Fruits, foliage and the evolution of primate colour vision. Philosophical Transactions of the Royal Society of London B– Biological Sciences, 356, 229–283.Google Scholar
  84. Remis, M. J. (2000). Initial studies on the contributions of body size and gastrointestinal passage rates to dietary flexibility among gorillas. American Journal of Physical Anthropology, 112, 171–180.PubMedGoogle Scholar
  85. Remis, M. J., Dierenfeld, E. S., Mowry, C. B., & Carroll, R. W. (2001). Nutritional aspects of western lowland gorilla (Gorilla gorilla gorilla) diet during seasons of fruit scarcity at Bai Hokou, Central African Republic. International Journal of Primatology, 22, 807–836.Google Scholar
  86. Robinson, B. W., & Wilson, D. S. (1998). Optimal foraging, specialization, and a solution to Liem’s paradox. American Naturalist, 151, 223–235.PubMedGoogle Scholar
  87. Rogers, M. E., Maisels, F., Williamson, E. A., Fernandez, M., & Tutin, C. E. G. (1990). Gorilla diet in the Lopé Reserve, Gabon: A nutritional analysis. Oecologia, 84, 326–339.Google Scholar
  88. Rosenberger, A. L. (1992). Evolution of feeding niches in new world monkeys. American Journal of Physical Anthropology, 88, 545–562.Google Scholar
  89. Rosenberger, A. L., & Kinzey, W. G. (1976). Functional patterns of molar occlusion in platyrrhine primates. American Journal of Physical Anthropology, 45, 281–298.PubMedGoogle Scholar
  90. Russon, A. E., & Begun, D. R. (2004). Evolutionary origins of great ape intelligence: An integrated view. In A. E. Russon & D. R. Begun (Eds.), The evolution of thought: Evolutionary origins of great ape intelligence (pp. 353–368). Cambridge, U.K.: Cambridge University Press.Google Scholar
  91. Schluter, D. (1994). Experimental evidence that competition promotes divergence and adaptive radiation. Science, 266, 798–801.PubMedGoogle Scholar
  92. Schoener, T. W. (1982). The controversy over interspecific competition. American Scientist, 70, 586–595.Google Scholar
  93. Steenbeek, R., & van Schaik, C. P. (2001). Competition and group size in Thomas’s langurs (Presbytis thomasi): The folivore paradox revisited. Behavioral Ecology Sociobiology, 49, 100–110.Google Scholar
  94. Surridge, A. K., Osorio, D., & Mundy, N. I. (2003). Evolution and selection of trichromatic vision in primates. Trends in ecology and evolution, 18, 198–205.Google Scholar
  95. Temerin, L. A., & Cant, J. G. H. (1983). The evolutionary divergence of Old World monkeys and apes. American Naturalist, 122, 335–351.Google Scholar
  96. Terborgh, J. (1983). Five new world primates. Princeton, NJ: Princeton University. Press.Google Scholar
  97. Terborgh, J. (1986). Keystone plant resources in the tropical forest. In M. Soulé (Ed.), Conservation biology: The science of scarcity and diversity (pp. 330–344) Sunderland, MA: Sinauer.Google Scholar
  98. Tomasello, M., & Call, J. (1997). Primate cognition. New York: Oxford University Press.Google Scholar
  99. Tutin, C. E. G., Fernandez, M., Rogers, M. E., Williamson, E. A., & McGrew, W. C. (1991). Foraging profiles of sympatric lowland gorillas and chimpanzees in the Lope Reserve, Gabon. Philosophical Transactions of the Royal Society of London B–Biological Sciences, 334, 179–186.Google Scholar
  100. Tutin, C. E. G., Ham, R. M., White, L. J. T., & Harrison, M. J. S. (1997). The primate community of the Lope Reserve, Gabon: Diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology, 42, 1–24.PubMedGoogle Scholar
  101. Ungar, P. S. (1996a). Relationship of incisor size to diet and anterior tooth use in sympatric Sumatran anthropoids. American Journal of Physical Anthropology, 38, 145–156.Google Scholar
  102. Ungar, P. S. (1996b). Feeding height and niche separation in sympatric Sumatran monkeys and apes. Folia Primatologica, 67, 163–168.Google Scholar
  103. Ungar, P. (2004). Dental topography and diets of Australopithecus afarensis and early Homo. Journal of Human Evolution, 46, 605–622.PubMedGoogle Scholar
  104. van Schaik, C. P., & Knott, C. D. (2001). Geographic variation in tool use on Neesia fruits in orangutans. American Journal of Physical Anthropology, 114, 331–342.PubMedGoogle Scholar
  105. van Schaik, C. P., Deaner, R. O., & Merrill, M. Y. (1999). The conditions for tool use in primates: Implications for the evolution of material culture. Journal of Human Evolution, 36, 719–741.PubMedGoogle Scholar
  106. van Schaik, C. P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, C. D., Singleton, I., et al. (2003). Orangutan cultures and the evolution of material culture. Science, 299, 102–105.PubMedGoogle Scholar
  107. Waser, P. M. (1987). Interactions among primate species. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 210–226). Chicago: University of Chicago Press.Google Scholar
  108. Watts, D. P. (1984). Composition and variability of mountain gorilla diets in the central Virungas. American Journal of Primatology, 7, 323–356.Google Scholar
  109. Watts, D. P. (1998). Seasonality in the ecology and life histories of mountain gorillas (Gorilla gorilla beringei). International Journal of Primatology, 19, 929–948.Google Scholar
  110. Watts, D. P., & Mitani, J. C. (2002). Hunting behavior of chimpanzees at Ngogo, Kibale National Park, Uganda. International Journal of Primatology, 23, 1–28.Google Scholar
  111. White, F. J. (1998). Seasonality and socioecology: The importance of variation in fruit abundance to bonobo sociality. International Journal of Primatology, 19, 1013–1027.Google Scholar
  112. Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., Sugiyama, Y., et al. (1999). Cultures in chimpanzees. Nature, 399, 682–685.PubMedGoogle Scholar
  113. Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262–300.Google Scholar
  114. Wrangham, R. W. (1986). Ecology and social relationships in two species of chimpanzee. In D. I. Rubenstein & R. W. Wrangham (Eds.), Ecology and social evolution: Birds and mammals (pp. 352–378). Princeton, NJ: Princeton University Press.Google Scholar
  115. Wrangham, R. W., Conklin-Brittain, N. L., & Hunt, K. D. (1998). Dietary response of chimpanzees and Cercopithecines to seasonal variation in fruit abundance: I. Antifeedants. International Journal of Primatology, 19, 949–970.Google Scholar
  116. Yamagiwa, J. (2004). Diet and foraging of the great apes: Ecological constraints on their social organizations and implications for their divergence. In A. E. Russon & D. R. Begun (Eds.), The evolution of thought: Evolutionary origins of great ape intelligence (pp. 210–233). Cambridge, U.K.: Cambridge University Press.Google Scholar
  117. Yamakoshi, G. (1998). Dietary responses to fruit scarcity of wild chimpanzees at Bossou, Guinea: Possible implications for ecological importance of tool use. American Journal of Physical Anthropology, 106, 283–295.PubMedGoogle Scholar
  118. Yamakoshi, G. (2004a). Food seasonality and socioecology in Pan: Are West African chimpanzees another bonobo? African Study Monographs, 25, 45–60.Google Scholar
  119. Yamakoshi, G. (2004b). Evolution of complex feeding techniques in primates: Is this the origin of great ape intelligence? In A. E. Russon & D. R. Begun (Eds.), The evolution of thought: Evolutionary origins of great ape intelligence (pp. 140–171). Cambridge, U.K.: Cambridge University Press.Google Scholar
  120. Yamashita, N. (1998). Functional dental correlates of food properties in five Malagasy lemur species. American Journal of Physical Anthropology, 106, 169–188.PubMedGoogle Scholar
  121. Yeager, C. P. (1989). Feeding ecology of the proboscis monkey (Nasalis larvatus). International Journal of Primatology, 10, 497–530.Google Scholar
  122. Yeager, C. P., & Kool, K. (2000). The behavioral ecology of Asian colobines. In P. F. Whitehead & C. J. Jolly (Eds.), Old world monkeys (pp. 496–521). Cambridge, U.K.: Cambridge University Press.Google Scholar

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Authors and Affiliations

  1. 1.Arnold Arboretum of Harvard UniversityCambridgeUSA
  2. 2.Department of Anthropology and Graduate Group in EcologyUniversity of CaliforniaDavisUSA
  3. 3.Department of AnthropologyHarvard UniversityCambridgeUSA

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